Neuromusculoskeletal Simulation Reveals Abnormal Rectus Femoris-Gluteus Medius Coupling in Post-stroke Gait

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Neuromusculoskeletal Simulation Reveals Abnormal Rectus Femoris-Gluteus Medius Coupling in Post-stroke Gait

Tunc Akbas, Richard R. Neptune and James Sulzer^*

• Walker Department of Mechanical Engineering, University of Texas at Austin, Austin, TX, United States

Post-stroke gait is often accompanied by muscle impairments that result in adaptations such as hip circumduction to compensate for lack of knee flexion. Our previous work robotically enhanced knee flexion in individuals post-stroke with Stiff-Knee Gait (SKG), however, this resulted in greater circumduction, suggesting the existence of abnormal coordination in SKG. The purpose of this work is to investigate two possible mechanisms of the abnormal coordination: (1) a reflex coupling between stretched quadriceps and abductors, and (2) a coupling between volitionally activated knee flexors and abductors. We used previously collected kinematic, kinetic and EMG measures from nine participants with chronic stroke and five healthy controls during walking with and without the applied knee flexion torque perturbations in the pre-swing phase of gait in the neuromusculoskeletal simulation. The measured muscle activity was supplemented by simulated muscle activations to estimate the muscle states of the quadriceps, hamstrings and hip abductors. We used linear mixed models to investigate two hypotheses: (H1) association between quadriceps and abductor activation during an involuntary period (reflex latency) following the perturbation and (H2) association between hamstrings and abductor activation after the perturbation was removed. We observed significantly higher rectus femoris (RF) activation in stroke participants compared to healthy controls within the involuntary response period following the perturbation based on both measured (H1, p < 0.001) and simulated (H1, p = 0.022) activity. Simulated RF and gluteus medius (GMed) activations were correlated only in those with SKG, which was significantly higher compared to healthy controls (H1, p = 0.030). There was no evidence of synergistic coupling between any combination of hamstrings and hip abductors (H2, p > 0.05) when the perturbation was removed. The RF-GMed coupling suggests an underlying abnormal coordination pattern in post-stroke SKG, likely reflexive in origin. These results challenge earlier assumptions that hip circumduction in stroke is simply a kinematic adaptation due to reduced toe clearance. Instead, abnormal coordination may underlie circumduction, illustrating the deleterious role of abnormal coordination in post-stroke gait.

Introduction

Following a stroke, individuals often experience significant impairments including muscle weakness, spasticity, increased tone, and abnormal coordination (1), which often results in compensatory movements (2). Abnormal coordination has been quantified in the upper limb (3), but only more recently in the lower limbs using joint torque measures (4–7), mechanical perturbations (7, 8) and H-reflex stimulations (9–12). However, it is unclear whether such abnormal coordination has direct consequences on gait function. Descriptive gait analyses based on biomechanical data and simulated muscle activations during gait in post-stroke individuals (13–15) and gait in cerebral palsy (16, 17) suggest that lack of lower limb coordination is related to gait dysfunction. Yet descriptive analysis lacks the ability to identify the mechanisms of abnormal coordination that perturbation methods can provide.

Our previous work developed a device that delivers controlled knee flexion torque perturbations during gait (18) and applied it to individuals post-stroke with Stiff-Knee Gait (SKG) (19). SKG is defined by reduced knee flexion during the swing phase, often assumed to be compensated for with hip circumduction (2). However, when exposed to pre-swing knee flexion torque perturbations, those with SKG walked with exaggerated hip abduction during swing instead of the expected reduction, while there was no change in healthy controls (19). Biomechanical factors such as balance and perturbation dynamics could not account for the increased abduction. These results suggested that hip abduction may not be solely acting as a compensatory motion for reduced knee flexion. We examined this possibility further by restricting knee flexion in healthy individuals with a knee brace (20). We observed that hip hiking, not abduction, compensated for reduced knee flexion, despite persistently high hip abduction in those with post-stroke SKG. Thus, abnormal neural behavior appears to underlie the hip abduction in people with SKG. However, the neural mechanisms leading to the exaggerated hip abduction remain unclear. The abnormal cross-planar kinematics were likely the result of abnormal heteronymous muscular activation initiated via reflexive (8) or voluntary (4, 21) mechanisms. For instance, cross-planar reflexive couplings between adductor longus (AL) and RF were observed in individuals post-stroke while in a seated position (8). Also in post-stroke individuals, voluntary activation of the hamstrings resulted in a cross-planar coupling with adductors while standing (4). This is in agreement with previous simulation analyses of post-stroke gait showing synergetic coupling between hip abductors and knee flexors in the swing phase (22). Based on this information, the exaggerated abduction observed in our previous work may have been the result of a reflexive stimulus of the RF coupled with abductor muscles (Hypothesis 1). In contrast, such abductor activity may have been coupled with voluntary initiation of the hamstrings (Hypothesis 2) as an adaptation to the perturbations.

In this work, we seek to delineate the underlying muscle activation behind the abnormal cross-planar kinematics. We used neuromusculoskeletal modeling and simulation (NMMS) to derive the estimated muscle states and supplement measured EMG. NMMS combines the use of a lower limb musculoskeletal model with measured kinematic and kinetic data to estimate muscle states (23, 24). Descriptive NMMS simulations have identified the role of rectus femoris in post-stroke gait (25). Here we used NMMS to estimate muscle states that are difficult to measure experimentally during gait, such as fiber stretch velocity and all lower limb muscle activities, including abductor muscles that are difficult to access using EMG. The accuracy of the simulated fiber stretch measures were obtained from Hill-type muscle models verified by muscle moment-arms of cadaver subjects (26–28). Simulated fiber length and velocity has been used for generating tunable models for contracture and spasticity assessments (29) and determining operating range of fibers during walking with different speeds (30, 31). Thus, together with measured EMG, NMMS can help elucidate mechanisms of cross-planar muscle synergies and abnormal reflexive responses. Evidence of an abnormal reflex coupling underlying excessive hip abduction during knee flexion perturbations in those with SKG would manifest itself as a hyperactive RF stretch reflex followed by heteronymous activation in the hip abductors (H1). Alternatively, if the abnormal coupling was generated by the voluntary knee flexion movement and due to lack of independent joint control, temporary removal of torque perturbations (“catch trials”) should result in correlated activation between the hamstrings and abductors (H2). This study represents a novel approach toward delineating the differential roles of impairments in post-stroke gait.